Livestock Foraging Behavior In Response To Sequence and Interactions Among Alkaloids, Tannins, and Saponins
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1 Utah State University All Graduate Theses and Dissertations Graduate Studies Livestock Foraging Behavior In Response To Sequence and Interactions Among Alkaloids, Tannins, and Saponins Tiffanny L. Jensen Utah State University Follow this and additional works at: Part of the Other Life Sciences Commons Recommended Citation Jensen, Tiffanny L., "Livestock Foraging Behavior In Response To Sequence and Interactions Among Alkaloids, Tannins, and Saponins" (2012). All Graduate Theses and Dissertations This Dissertation is brought to you for free and open access by the Graduate Studies at It has been accepted for inclusion in All Graduate Theses and Dissertations by an authorized administrator of For more information, please contact
2 LIVESTOCK FORAGING BEHAVIOR IN RESPONSE TO SEQUENCE AND INTERACTIONS AMONG ALKALOIDS, TANNINS, AND SAPONINS by Tiffanny L. Jensen A dissertation submitted in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY in Range Science Approved: Frederick D. Provenza Juan J. Villalba Major Professor Committee Member Randall D. Wiedmeier Carl D. Cheney Committee Member Committee Member Kevin Welch Mark R. McLellan Committee Member Vice President for Research and Dean of the School of Graduate Studies UTAH STATE UNIVERSITY Logan, Utah 2012
3 ii Copyright Tiffanny Jensen 2012 All Rights Reserved
4 iii ABSTRACT Livestock Foraging Behavior in Response to Sequence and Interactions Among Alkaloids, Tannins and Saponins by Tiffanny Lyman Jensen, Doctor of Philosophy Utah State University, 2012 Major Professor: Dr. Fredrick D. Provenza Department: Wildland Sciences The influence of primary compounds (energy, protein, minerals, and vitamins) in animal nutrition and foraging behavior has been studied for years. The roles of secondary compounds (terpenes, alkaloids, and phenolic compounds) are equally important, yet they have been ignored until recently. Where secondary compounds were once considered toxic by-products of plant metabolism, we now know they are actively involved in plant and animal behavior, health, and productivity. Though often appreciated historically for their negative impacts on food intake and animal production, we are becoming increasingly aware of their beneficial roles in the health of plants, animals, and humans. When animals can ingest an array of plants that contain different kinds and amounts of secondary compounds, they can mix different foods in their diet to better use both primary and secondary compounds, enhancing their health and production, as well as economic and ecological characteristics of landscapes. Endophyte-infected tall fescue contains the alkaloids perlolidine, perloline, ergotamine, and ergovaline, which are all steroidal or protein-like in nature. Tannins and saponins have a high
5 iv affinity for binding proteins and lipids in the gastro-intestinal tract of animals, and facilitating their excretion from the body. These findings suggest animals may increase their use of forages with alkaloids when they are also provided forages that contain tannins or saponins. The sequence in which forages with different secondary compounds are ingested may influence any potential interactions because different compounds have different residence times in the gastrointestinal tract. I tested the hypothesis that cattle and sheep foraging behavior is influenced by eating different combinations of forages containing secondary compounds in different sequences. In pen and pasture trials, I showed that 1) cattle grazing pastures of endophyte-infected tall fescue (TF) grazed more often on TF when first allowed to graze legumes containing either tannins or saponins, and they grazed TF much more when they first grazed legumes as opposed to the reverse sequence; 2) sheep fed basal diets high in the alkaloid ergotamine d tartrate (EDT) ate more when supplemented with food containing either tannins or saponins, but in contrast to the trials on pasture with cattle, their behavior was not dramatically influenced by sequence; 3) cattle fed fresh cut endophyte-infected tall fescue were not influenced by the addition of tannin to their drinking water, as tannins limited both water and forage intake; 4) sheep fed food containing EDT ate more when supplemented with food containing tannins or when given a choice of foods containing tannins or saponins, than sheep supplemented with food containing saponins or no additional secondary compound. Results from these studies suggest that secondary compounds interact with one another to influence foraging behavior, and that sequence of food ingestion can be influential when animals graze on pastures. (109 pages)
6 v PUBLIC ABSTRACT Livestock Foraging Behavior in Response to Sequence and Interactions Among Alkaloids, Tannins, and Saponins by Tiffanny L. Jensen, Doctor of Philosophy During the past several decades, people worldwide have expressed a growing interest in reconstructing ecosystems to enhance ecological, economic, and social values. Yet, to do so we must find ways to enhance biodiversity, environmental quality and the sustainability of grazing lands. In all these instances, plants are the glue that binds soils, water, herbivores, and people. However, monocultures or simple grass-legume mixtures are not always ideal for intensively managed pastures due to their seasonality, susceptibility to pests, and monotony of plant nutrients and toxins. All plants contain so-called toxins, more appropriately referred to as secondary compounds, which are crucial in plant defense and survivability. High doses of secondary compounds can cause decreases in animal intake, production, and health, dramatically impacting the efficiency and cost of livestock production and land management. Yet, diverse mixtures of plants may provide many benefits monocultures cannot. Complementarities among plant secondary compounds may actually enhance animal intake, efficiency and health when animals eat plants that contain higher levels of secondary compounds (i.e. toxins). With my PhD program, I sought to understand how complementary interactions among the secondary compounds alkaloids, tannins, and saponins influenced livestock grazing behavior and the further implications of these interactions for land and animal management. This
7 vi research will help us better understand the ability of herbivores to use complementary forages to enhance the biodiversity of landscapes and productivity of herbivores while at the same time decreasing our reliance on herbicides and insecticides to protect plants. Complementary foods and sequence in animal grazing systems may prove fundamental in the upcoming transition from high fossil fuel inputs to more sustainable alternatives in animal and land management.
8 vii ACKNOWLEDGMENTS This research was supported by grants from the Utah Agricultural Experiment Station, BEHAVE, the Quinney Scholarship Fund, and the Pasture Initiative, Utah State University. Thank you for your funding and support. I d like to thank my major professor, Fred Provenza, for all the encouragement and help with completing my doctoral program. You have been a great mentor and a wonderful friend. Thank you for allowing me to work with you. I d also like to thank Juan Villalba for his continued guidance and support throughout the last few years. Thank you for your willingness to help me when I needed it. You are a wonderful friend and mentor, and I have greatly enjoyed working with you. Thanks to Carl Cheney, Kevin Welch, and Randy Wiedmeier for being great committee members and helping to widen my understanding of the world around us. I have enjoyed getting to know each of you during this process, and appreciate your friendship and support. Many thanks go to Rae Ann Hart and Beth Burritt, who both have been incredible friends willing to give me all the free advice and help I could ask for. Thanks for your help! I d also like to thank Dave Forrester, Don Synder, and the crew in Lewiston for your help and assistance with the facilities and pastures. Further thanks go to the Poisonous Plants Research Facility for their great help in analyzing plant compounds, and allowing me to use their Richmond research facility. And last, but not least, special thanks to my family for their love and support! Thank you, thank you, thank you for sustaining me in this path, and allowing me to express my passion for livestock behavior and sustainable agriculture. Tiffanny L. Jensen
9 viii CONTENTS Page ABSTRACT... iii PUBLIC ABSTRACT... v ACKNOWLEDGMENTS... vii LIST OF TABLES... x LIST OF FIGURES...xi CHAPTER 1. INTRODUCTION... 1 References CATTLE PREFERENCES DIFFER WHEN FORAGES CONTAINING ALKALOIDS, TANNINS, OR SAPONINS ARE GRAZED IN DIFFERENT SEQUENCES... 7 Abstract... 7 Introduction... 8 Materials and Methods... 9 Results Discussion Implications References INFLUENCE OF DIET SEQUENCE ON INTAKE OF FOODS CONTAINING ERGOTAMINE D TARTRATE, TANNINS, AND SAPONINS BY SHEEP Abstract Introduction Materials and Methods Results Discussion Conclusion References INFLUENCE OF DRINKING WATER WITH TANNIN ON INTAKE OF ENDOPHYTE- INFECTED TALL FESCUE BY CATTLE Abstract... 44
10 ix Introduction Materials and Methods Results Discussion Conclusion References INTAKE OF FOOD CONTAINING ERGOTAMINE D TARTRATE BY SHEEP OFFERED FOODS WITH TANNINS OR SAPONINS OR A CHOICE OF TANNINS AND SAPONINS Abstract Introduction Materials and Methods Results Discussion Conclusion References CONCLUSIONS AND IMPLICATIONS: FOOD COMPLEMENTARITIES, SYNERGYS AND SEQUENCES Overview of My Research Complementarities among Primary and Secondary Compounds in Foods Sequence of Food Ingestion Influences Foraging Behavior Food Synergies in Human Diets Importance of Complementarities in Livestock and Land Management Practical Implications and needs for Research References APPENDIX... 96
11 x LIST OF TABLES Table Page 1 Plant chemical analyses (means ± std. errors) for neutral detergent fiber (NDF), nitrogen (N), and for alkaloids (endophyte-infected tall fescue, Festuca arundinaceum, Kentucky 31), tannins (birdsfoot trefoil, Lotus corniculatus variety Goldie) and saponins (alfalfa, Medicago sativa variety Vernal... 14
12 xi LIST OF FIGURES Figure Page 1 Depiction of one pasture unit containing adjacent monoculture pastures of Tall Fescue (TF) Alfalfa (ALF), and Birdsfoot Trefoil (BFT) with Orchard Grass (OG) holding areas Within each pasture unit were 2 sequence treatments (Seq 1: TF BFT or ALF and Seq 2: BFT or ALF TF) Percent scans heifers spent grazed tall fescue (TF) before or after a meal of birdsfoot trefoil (BFT) (A and B), or alfalfa (ALF) (C and D) in 4 phases. Phases 1 and 3 lasted 10 d, whereas Phases 2 and 4 lasted 5 d. Cattle first grazed TF for 45 min followed by a meal of BFT (A and B) or ALF (C and D) for 45 min or they first grazed BFT (A and B) or ALF (C and D) for 45 min followed by TF for 45 min. Bars are standard errors Intake of food containing ergotamine d tartrate (EDT) by sheep during Experiment 1. Sheep were supplemented with food containing tannins before EDT food (TAN EDT), with tannin after EDT (EDT TAN), or with only EDT (EDT EDT). Bars are standard errors Intake of food containing ergotamine d tartrate (EDT) by sheep during Experiment 2. Sheep were supplemented with food containing saponins before EDT food (SAP EDT), with saponin after EDT (EDT SAP), or with only EDT (EDT EDT). Bars are standard errors Intake of supplemental food containing tannins (TAN) by sheep offered foods in two sequences (TAN-->EDT or EDT TAN) during Experiment 1. Bars are standard errors Intake of supplemental food containing saponins (SAP) offered foods in two sequences (SAP-->EDT or EDT SAP) by sheep during Experiment 2. Bars are standard errors Intake of fresh water or water containing 1% condensed tannins by cattle. Bars are standard errors Intake of fresh cut Endophyte-Infected Tall Fescue by cattle offered fresh water or fresh water containing 1% tannin. Bars are standard errors Intake of food containing ergotamine d tartrate (EDT), tannin (TAN), saponin (SAP) or no additional SC (CNT) by sheep during Feeding Period 1. Sheep were supplemented with a CHOICE, TAN, SAP, or CNT before EDT. Bars are standard errors Intake of food containing ergotamine d tartrate (EDT), tannin (TAN), saponin (SAP) or no additional SC (CNT) by sheep during Feeding Period 2. Sheep were supplemented with a CHOICE, TAN, SAP, or CNT before EDT. Bars are standard errors... 60
13 xii 11 Intake of food containing EDT by sheep across days. Bars are standard errors Intake of food containing tannin (TAN), saponin (SAP) a choice of TAN and SAP (CHOICE) or no additional SC (CNT) by sheep during Feeding Period 1 and 2. Bars are standard errors... 61
14 CHAPTER 1 INTRODUCTION Life sustains life through myriad interactions among soils, plants, animals, and people. These interactions impact all aspects of agriculture, natural resource management, and human health. Chemical and microbial interactions in soils influence the biological workings of plants which then influences the nutrition and behavior of animals, which further impacts the health and vitality of people. Reconstructing ecosystems to enhance ecological, economic, and social values relies on the understanding and appreciating the complex interactions involved in the biodiversity and sustainability of natural resources. Most agricultural production in the Intermountain West revolves around livestock grazing pastures and rangelands. While commonly encouraged historically, planting monocultures or simple grass-legume mixtures is not always ideal for intensively managed pastures, because of their seasonality, susceptibility to pests, and monotony of their nutrient profiles. Diverse mixtures of plants may provide benefits monocultures cannot. For instance, more diverse mixtures of plants are likely to capture and use nitrates that accumulate in the root zone during the growing season, so they are not leached by winter precipitation (MacAdam, 2002). A diverse mix of species may add biochemical structure, nutrient diversification, and cover during times of the year when such resources may be absent if producers rely on monocultures. Furthermore, diverse mixtures of plants allow individual animals to select foods to meet their unique dietary needs, benefiting the physical health of the animal, the environmental health of landscapes, and the economic health of the producer. Plants and herbivores interact one with another in complex and often subtle ways mediated by interactions among primary (PC) and secondary compounds (SC). Primary
15 2 compounds (energy, protein, minerals and vitamins) directly influence the nutritional status of an animal. So-called SC (alkaloids, terpenes, and phenolics), formerly thought to be waste products of plant metabolism, are involved in plant defense, attracting pollinators, and a variety of other plant functions (Rosenthal and Berenbaum, 1992). Environmental factors, including herbivory and availability of nutrients, water, and light, influence the evolution (Coley et al., 1985) and phenotypic expression (Bryant et al., 1983) of SC, which then influence how SC interact with soils, plants, herbivores, and people (Provenza, 2008). Historically, ecologists emphasized the role of SC in plant defense and herbivore behavior. Most SC limit how much of a particular plant species an herbivore can eat, thereby spreading the load of herbivory across many species and encouraging herbivores to eat a variety of plants (Freeland and Janzen, 1974, Foley et al., 1999). Post-ingestive feedback mechanisms assist animals in limiting the dose of primary or SC to avoid toxicosis (Provenza, 1995, 1996; Foley et al., 1999). For instance, oral gavages of toxins cause dose-dependent decreases in intake of foods that contain the toxins (Wang and Provenza, 1997). Yet, herbivores are able to eat more when given a variety of food with different kinds of SC as different SC affect the body in different ways and are detoxified by different mechanisms (Freeland and Janzen, 1974). A diverse intake of SC may also lead to neutralization or inactivation of the compound, which in turn could reduce susceptibility to toxic doses. Interactions among plants with SC can lead to complementary relationships such that eating a combination of foods may exceed the benefit of consuming any one food in isolation (Tilman, 1982). When sheep choose between foods that contain either amygdaline or lithium chloride, they eat more than lambs offered a food that contains only one of these compounds; the same is true with nitrate and oxalate (Burritt and Provenza, 2000). Sheep eat more when
16 3 offered three foods that contain terpenes, tannins, and oxalates than when offered foods with only one or two of these compounds (Villalba et al., 2004). They also eat more food containing alkaloids when supplemented with foods containing tannins or saponins than when only given a food with alkaloids (Lyman et al., 2008). Mule deer eat more when offered both sagebrush and juniper (12.3 g/kg BW), plants that contain different phenolics and terpenes, than when they are offered only sagebrush (4.2 g/kg BW) or juniper (7.8 g/kg BW) (Smith, 1959). Brushtail possums that can select from two diets containing phenolics and terpenes eat more food than when they consume diets containing only one of these compounds (Dearing and Cork, 1999), and the same is true in principle with squirrels (Schmidt et al., 1998). The sequence in which complementary foods are ingested also influences preference. Sheep eat more terpene-containing foods after a meal of tannin-containing foods than when the sequence is reversed (Mote et al., 2008). Cattle graze more on endophyte-infected tall fescue (containing alkaloids) when first allowed to graze on legumes containing tannins or saponins than when the sequence was reversed (Lyman et al., 2011), and sheep decrease intake of tall fescue in a meal, unless they receive an oral gavage of tannins prior to the meal, in which case they eat tall fescue throughout the meal (Lisonbee, 2009). Thus, while animals can meet needs for PC and tolerate higher total intake of SC when they can choose from a variety of plants (Provenza and Villalba, 2006), outside of the aforementioned studies, very little is known about which SC in plants are complementary and which are not when different forages are ingested in different sequences. In their efforts to describe the defensive roles of SC in plants, researchers have not considered their possible health benefits (Engel, 2002). Everything depends on concentration: PCs and SCs at too high concentrations can be toxic, while at lower concentrations they can both
17 4 have health benefits (Provenza and Villalba, 2006). Likewise, in our haste to increase the palatability of monoculture pasture species, researchers and producers have selected for low concentrations of compounds such as alkaloids (reed canary grass and endophyte-infected tall fescue), tannins (birdsfoot trefoil), and saponins (alfalfa), not appreciating that these compounds in proper mixtures may actually benefit both plants and animals. My objectives were to test the hypothesis that cattle and sheep foraging behavior is influenced by eating different combinations and sequences of forages containing SC. Specifically I determined: 1) if cattle ate more endophyte-infected tall fescue after first grazing on legumes containing either tannins (birdsfoot trefoil) or saponins (alfalfa) than cattle grazing in the reverse sequence; 2) if sheep fed a food containing an alkaloid (ergotamine d tartrate) ate more when first supplemented with food containing either tannins or saponins than when fed in the reverse sequence; 3) if cattle ate more freshly cut endophyte-infected tall fescue when supplemented with tannin added to their water than cattle only given fresh water; 4) and if sheep varied their intake of foods containing ergotamine d tartrate, tannins, and saponins when given in various combinations and sequences. REFERENCES Bryant, J.P., F.S. Chapin III, and D.R. Kline Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357. Burritt, E.A., and F.D. Provenza Role of toxins in intake of varied diets by sheep. J. Chem. Ecol. 26:1991. Coley, P.D., J.P. Bryant, and F.S. Chapin III Resource availability and plant antiherbivore defense. Science 230:895.
18 5 Dearing, M.D., and S. Cork Role of detoxification of plant secondary compounds on diet breadth in a mammalian herbivore, Trichosurus vulpecula. J. Chem. Eco. 25:1205. Engel, C Wild Health. Houghton Mifflin Co., Boston, New York, NY. Foley, W.J., G.R. Iason, and C. McArthur Role of plant secondary metabolites in the nutritional ecology of mammalian herbivores: How far have we come in 25 years? In: Freeland, W.J., and D.H. Janzen Strategies in herbivory by mammals: The role of plant secondary compounds. Am. Nat. 108:269. Lisonbee, L.D., J.J. Villalba, and F.D. Provenza Effects of tannins on selection by sheep of forages containing alkaloids, tannins and saponins. J. Sci. Food Agric. 89: Lyman, T.D., F.D. Provenza, and J.J. Villalba Sheep foraging behavior in response to interactions among alkaloids, tannins and saponins. J. Sci. Food Agric. 88: Lyman, T.D., F.D. Provenza, J.J. Villalba, and R.D. Wiedmeier Cattle preferences differ when endophyte-infected tall fescue, birdsfoot trefoil, and alfalfa are grazed in difference sequences. J. Anim. Sci. 89:1131. MacAdam, J.W Grass and forage legume mixes what s hot and what s not! In: J.E. Brummer and C.H. Pearson (Ed.) Proc. Intermountain Forage Symp. pp Colorado State Univ., Tech. Bull. LTB Mote, T. E., J. J. Villalba, and F. D. Provenza Sequence of food presentation influences intake of foods containing tannins and terpenes. Appl. Anim. Behav. Sci. 113: Provenza, F.D Postingestive feedback as an elementary determinant of food preference and intake in ruminants. J. Range Manage. 48:2. Provenza, F.D Acquired aversions as the basis for varied diets of ruminants foraging on rangelands. J. Anim. Sci. 74:2010.
19 6 Provenza, F.D What does it mean to be locally adapted and who cares anyway? J. Anim. Sci. 86:E271-E284. Provenza, F.D., and J.J. Villalba Foraging in domestic vertebrates: Linking the internal and external milieu. In: V.L. Bels (Ed.) Feeding in Domestic Vertebrates: From Structure to Function. CABI Publ., Oxfordshire, UK. Rosenthal, G.A. and M.R. Berenbaum (eds.) Herbivores: Their Interactions with Secondary Plant Metabolites. (2 nd Ed.). Academic Press, New York. Schmidt, K.S., L.S. Brown, and R.A. Morgan Plant defense as complementary resources: a test with squirrels. Oikos 81:130. Smith, A.D Adequacy of some important browse species in overwintering mule deer. J. Range. Manage. 12:9. Tilman, D Resource Competition and Community Structure. Princeton Univ. Press, Princeton, NJ. Villalba, J.J., F.D. Provenza and H. GouDong Experience influences diet mixing by herbivores: Implications for plant biochemical diversity. Oikos 107:100. Wang, J. and F.D. Provenza Dynamics of preference by sheep offered foods varying in flavors, nutrients, and a toxin. J. Chem. Ecol. 23:275.
20 7 CHAPTER 2 CATTLE PREFERENCES DIFFER WHEN ENDOPHYTE-INFECTED TALL FESCUE, BIRDSFOOT TREFOIL, AND ALFALFA ARE GRAZED IN DIFFERENCE SEQUENCES 1 Abstract We determined if sequence of ingestion affected use of endophyte-infected tall fescue (TF) when cattle also grazed either birdsfoot trefoil (BFT) or alfalfa (ALF). Based on chemical characteristics of TF (alkaloids), BFT (tannins), and ALF (saponins), we hypothesized that cattle first allowed to graze ALF or BFT would subsequently spend more time grazing TF than cattle that first grazed TF followed by ALF or BFT. Sixteen bred heifers (478± 39 kg initial BW) were randomly assigned to 4 replicated pasture units. Each replicated unit consisted of 4 treatment sequences (TF BFT, TF ALF, BFT TF, or ALF TF), with 2 cows per sequence. Pastures were in the vegetative stage of growth at a height of 20 to 30 cm and provided ad libitum forage to cattle. We recorded foraging on TF, BFT and ALF using scan sampling of individuals at 2-min intervals. The study was conducted in 4 phases run sequentially, for a total of 30 d. In phases 1 and 3, cattle in Group 1 grazed TF pastures for 45 min and were then moved to BFT pastures for the next 45 min (TF BFT); cattle in Group 2 grazed in the reverse sequence (BFT TF). Inphases 2 and 4, cattle in Group 1 grazed TF pastures for 45 min and then subsequently grazed ALF pastures for the remaining 45 min (TF ALF); cattle in Group 2 grazed in the reverse 1 Chapter 2 Coauthored by Tiffanny Lyman Jensen, Frederick D. Provenza, and Juan J. Villalba. J. Anim. Sci. published online Nov. 5, Copyright [2012] American Society of Animal Science.
21 8 sequence (ALF TF). Sequence of plant ingestion affected food selection. In phase 1, scans revealed grazing of TF by heifers was cyclic, and heifers tended to have more scans grazing TF when they grazed BFT TF; scans for heifers grazing TF were consistently ALF TF spent considerably more scans foraging on TF from d 4-10 than heifers that grazed in the sequence TF ALF, and they remained higher throughout Phase 4 of the trial. While the sequence ALF TF appeared to be more effective than BFT TF, consistent with the hypothesis of a complementary relationship between the steroidal alkaloids in TF and saponins in ALF, tannin concentrations in BFT were low (1.8%), which likely reduced the presumed inactivation of alkaloids by tannins. We also speculate heifers needed to learn about the positive postingestive influence of sequence, a notion consistent with more similar scans spent foraging BFT and TF early in Phases 1 (BFT TF) and 2 (ALF TF), and with the consistent and marked increase in scans spent foraging on TF for animals foraging in Phases 3 (BFT TF) and 4 (ALF TF). INTRODUCTION Little is known about how the sequence of food ingestion influences forage intake and preference, though it appear to be important. Sheep eat more when foods with secondary compounds are offered in the morning followed by limited nutritious foods in the afternoon (Papachristou et al., 2007). Sheep also eat more food with terpenes when they first eat food with tannins (Mote et al., 2008); food with tannins eaten first remains in the gut up to 72 hours (Silanikove et al., 1994), where tannins can interact with terpenes, whereas terpenes are highly soluble compounds absorbed quickly from the gastrointestinal tract and eliminated from the body (Foley and McArthur, 1994). Altering the sequence of forage ingestion also causes calves
22 9 to spend more time eating grasses such as endophyte-infected tall fescue and reed canarygrass when they first eat legumes such as alfalfa or birdsfoot trefoil and then eat endophyte-infected tall fescue or reed canarygrass (Lyman, 2008). Our objective in the present study was to follow-up on the study of Lyman (2008), which was more elaborate in the choices offered to fall-born calves, with a specific focus on foraging sequence and more limited choices offered to bred heifers. To do so, we determined if the sequence of grazing endophyte-infected tall fescue (TF) and legumes containing tannins (birdsfoot trefoil, BFT) or saponins (alfalfa, ALF) increased use of TF by bred heifers. The alkaloids in TF are protein-like and steroidal in nature, whereas the tannins in BFT and the saponins in ALF are high molecular weight compounds, not absorbed through the rumen wall, with high affinity for binding to protein and lipid-like compounds such as the alkaloids in TF (Malinow et al., 1979; Jones and Mangan, 1977). We thus hypothesized cattle would eat more TF after eating forages with tannins (BFT) or saponins (ALF). MATERIALS AND METHODS Chemical Characteristics of Plant Species. Alkaloids are small, fat-soluble molecules absorbed rapidly through the rumen epithelium. In high amounts, they can decrease food intake and animal performance (Cheeke and Schull, 1985). Tall fescue contains two groups of alkaloids, one associated with the plant and the other allied with the fungus Neotyphodium coenophialum. The intrinsic alkaloids perlolidine and perloline, which are steroidal, negatively affect rumen fermentation and food intake. The fungus-associated alkaloids N-acetylloline, N-formylloline, ergotamine and ergovaline, which have lipid structures, reduce food intake and cause fescue toxicity.
23 10 Conversely, tannins and saponins are high-molecular-weight compounds (2,000 to 4,000) that remain in the gut for many hours where they interact with many other compounds (Kumar and Singh, 1984; Min and Hart, 2003). Condensed tannins in plants like BFT bind to proteins in the rumen (Jones and Morgan, 1977); as alkaloids are nitrogen-based, we hypothesized including tannin-containing BFT in the diets of livestock would neutralize the alkaloids in TF, and stable complexes form between alkaloids and tannins (Okuda et al., 1982; Wong and Provenza, unpublished data). Saponins in plants like alfalfa bind to lipids such as cholesterol in the gastrointestinal tract of animals causing their excretion in the feces (Malinow et al., 1979); as the endogenous alkaloids in TF are lipid, we hypothesized including ALF in the diet of animals grazing TF would also neutralize the alkaloids in TF. Given the rapid rate of absorption of alkaloids relative to tannins and saponins, we hypothesized that first grazing BFT or ALF would increase concentrations of tannins and saponins in the rumen and enable heifers to better use TF. Pasture Design. Plant species with alkaloids, tannins, and saponins were seeded at the Utah Agricultural Experiment Station Pasture Research Facility in Lewiston, UT (41 57 N W.). In 2006, we planted monocultures of tall fescue (TF) (Festuca arundinaceae, Kentucky 31 endophyte-infected) (Rottinghaus et al., 1991) with high concentrations of alkaloids, birdsfoot trefoil (BFT) (Lotus corniculatus variety Goldie) with high tannins (Hedqvist et al., 2000; Terrill et al., 1992), and alfalfa (ALF) (Medicago sativa varieties Vernal and Lahontan) with high saponins (Pedersen, 1975; Pedersen et al., 1976). Pasture units, constructed with temporary electric fence, consisted of a 0.05 ha plot of TF, a 0.04 ha plot of ALF and a 0.04 ha plot of BFT planted in adjacent monoculture strips, with 2.25 ha of orchard grass (OG) as a holding area (Figure 1). We had 4 replications of each unit with the
24 11 following sequences of grazing: 1) TF followed by ( ) ALF or BFT (Sequence 1), and 2) ALF or BFT followed by ( ) TF (Sequence 2). Grazing Trials. Sixteen bred 2-yr-old Black Angus heifers (478± 39 kg initial BW) were used in all phases of the trials. We randomly assigned 4 heifers to each of the 8 pasture units, with 2 heifers in each sequence within a unit. Each morning, cattle were moved from adjacent OG pastures to trial pastures for their morning meals. After each morning trial, cattle were moved back into OG pastures, where water and mineral supplements were provided. Pastures were in the vegetative stage of growth at a height of 20 to 30 cm and all plots provided ad libitum forage to cattle. Cattle were weighed pre- and post-trial to estimate changes in body weight during the 30-d trials. Procedures followed the protocols for animal care and use (IACUC protocol approval number 1372). Phase 1: Tall Fescue and Birdsfoot Trefoil. In the first phase, which lasted 10 d, cattle in Group 1 grazed TF pastures for 45 min and were then moved to BFT pastures for the next 45 min (Sequence 1 TF BFT). Cattle in Group 2 grazed in the reverse sequence (Sequence 2 BFT TF). OG TF ALF BFT 73.6' OG TF ALF BFT 73.6' 150' 76' 19' 19' Figure 1. Depiction of one pasture unit containing adjacent monoculture pastures of Tall Fescue (TF), Alfalfa (ALF), and Birdsfoot Trefoil (BFT) with Orchard Grass (OG) holding areas. Within each pasture unit were 2 sequence treatments (Seq 1: TF BFT or ALF and Seq 2: BFT or ALF TF).
25 12 Phase 2: Tall Fescue and Alfalfa. In the second phase, which also lasted 10 d, cattle in Group 1 grazed TF pastures for 45 min and then subsequently grazed ALF pastures for the remaining 45 min (Sequence 1 TF ALF). Cattle in Group 2 grazed in the reverse sequence (Sequence 2 ALF TF). Phase 3: Tall Fescue and Birdsfoot Trefoil (5 d). Given the experience animals gained in Phase 1, we wanted to determine if their behavior was similar in Phase 3 to that exhibited in Phase 1. The third phase thus consisted of one 5-d period where cattle in Group 1 first grazed TF pastures for 45 min and then grazed BFT for 45 min for a 5 d period (Sequence 1 TF BFT). Cattle in Group 2 grazed in the reverse sequence (Sequence 2 BFT TF). Phase 4: Tall Fescue and Alfalfa (5 d). Given the experience animals gained in Phase 2, we wanted to determine if their behavior was similar in Phase 4 to that exhibited in Phase 2. The fourth phase thus consisted of another 5-d period where cattle in Group 1 first grazed TF pastures for 45 min and then grazed ALF for 45 min for a 5 d period (Sequence 1 TF ALF). Cattle in Group 2 grazed in the reverse sequence (Sequence 2 ALF TF). Scan Samples. In all phases of the study, one observer recorded behavioral data using scansamples of individually marked animals at 2-min intervals throughout daily trials from 0600 to 1030 each day (Altman, 1974). Scans were taken from a 3 m high platform centrally located to enable the observed to see all of the animals and whether or not they were grazing a particular forage. Animals were considered to be grazing only when they were actually biting and chewing forage; no grazing scan was recorded if an animal had its head in the sward, but was not biting or chewing forage. We then calculated the percent of scans each animal spent grazing each forage each day.
26 13 Chemical Composition of the Forages. Representative forage samples, collected from plants along a paced transect across each pasture, were hand-harvested at the end of the study, placed in plastic bags covered with dry ice immediately after harvest, and transported to a freezer where they were kept at -20 o C. They were subsequently freeze dried, ground through a Wiley mill with a 1-mm screen, and analyzed for neutral detergent fiber (NDF; Goering and Van Soest, 1970) and nitrogen (Method , AOAC, 2002), as well as condensed tannins (BFT) (Terrill et al., 1992), saponins (ALF) (Lee et al., 2001) and the alkaloid ergovaline (TF) (Rottinghaus et al., 1991). Statistical Design. The statistical design for the analysis of variance was a repeated measures with 4 replications of 2 sequences (TF legume or legume TF). Day was the repeated measure. Separate analyses were carried out for phases 1, 2, 3, and 4. The response variable was percent of scans observed per forage. RESULTS Chemical Composition of the Forages. Tall fescue contained more fiber and less N than either ALF or BFT (Table 1). Tall fescue was high in ergovaline, and ALF contained high amounts of saponins, but BFT was low in tannins (Table 1). Phase 1. Percent scans grazing TF did not differ between groups when cattle grazed TF BFT or BFT TF. Heifers spent 36% of the scans grazing TF in the sequence TF BFT and 45% of the scans grazing TF in the sequence BFT TF (P = 0.52, Figure 2A). Nor did scans spent grazing BFT differ (TF BFT= 98% vs. BFT TF = 96%, P = 0.27). Neither day (P = 0.36) nor day x sequence differed (P = 0.27).
27 14 Phase 2. The percent scans grazing TF differed between groups when heifers grazed TF ALF as opposed to ALF TF. Heifers spent 28% of the scans grazing TF in the sequence TF ALF and 51% of the scans grazing TF in the sequence ALF TF (P =0.03, Figure 2C). Groups did not differ in scans grazing ALF (TF ALF= 98% vs. ALF TF= 98%, P = 0.52). Day (P <0.0001) and day x sequence (P = 0.03) differed. Phase 3. When heifers grazed TF and BFT a second time, the percent of scans grazing TF tended to differ between groups for TF BFT and BFT TF. Heifers grazed 37% of the scans on TF in the sequence TF BFT and 61% of the scans on TF in the sequence BFT TF (P = 0.18, Figure 2B). Groups did not differ in scans grazing BFT (BFT TF =98%, TF BFT = 95%, P= 0.27). Day (P<0.05) differed, but no day x sequence interaction was observed (P = 0.27). Table 1: Plant chemical analyses (means ± std. errors) for neutral detergent fiber (NDF), nitrogen (N), and for alkaloids (endophyte-infected tall fescue, Festuca arundinaceae, Kentucky 31), tannins (birdsfoot trefoil, Lotus corniculatus variety Goldie) and saponins (alfalfa, Medicago sativa variety Vernal). Plant Species NDF, % N, % Total Condensed Saponins, % Ergovaline, ppb Tannins, % Birdsfoot Trefoil 44.1± ± ± Alfalfa 42.2± ± ± Tall Fescue 59.8± ± ±52.7
28 15 Phase 4. When heifers grazed TF and ALF a second time, the percent of scans grazing TF differed between groups for TF ALF and ALF TF. Heifers grazed 55% of the scans on TF in the sequence TF ALF and 85% of the scans on TF in the sequence ALF TF (P = 0.05, Figure 2D). Groups did not differ in scans grazing ALF (ALF TF =98%, TF ALF = 98%, P= 0.52). Day differed (P<0.01), but there was no day x sequence interaction (P = 0.67). Weight gains. Cattle gained an average of 0.95 ± 0.54 kg/head/d. DISCUSSION We determined if foraging sequence and plant diversity enhanced use of TF when cattle foraged on legumes that contained tannins (BFT) or saponins (ALF), and we found that forage species and sequence of forage ingestion affected food selection. Scans spent grazing TF were cyclic, especially when heifers grazed TF BFT in Phase 1, and they tended to spend more scans grazing TF when they grazed BFT TF, particularly on d 3, 5, 7, 9 and 10 of Phase 1 (Figure 2A); importantly, scans spent grazing BFT were consistently higher throughout Phase 3 of the trial (Figure 2B), which is consistent with previous findings when calves grazed significantly more in the sequence BFT TF than TF BFT (Lyman, 2008). In Phase 2, heifers that grazed in the sequence ALF TF spent considerably more scans foraging on TF from d 4-10 compared with heifers that grazed in the sequence TF ALF, and they remained higher throughout Phase 4 of the trial (Figures 2C and 2D). Scans spent grazing TF increased throughout the trials for animals grazing BFT TF and ALF TF, though heifers consistently grazed less on TF plots in phase 1 (BFT TF) than in phase 2 (ALF TF) (Figure 2A and 2C). Thus, while the sequence ALF TF appeared to be more effective than BFT TF, consistent with the hypothesis of a complementary relationship
29 16 between the steroidal alkaloids in TF and saponins in ALF, tannin concentrations in BFT were low (1.8%), which may have reduced the presumed tannin-alkaloid interactions. Tannin concentrations of 6-10% appear to be most effective at influencing grazing behavior without causing any harmful effects on intake or performance (Jones and Mangan, 1977; Lyman et al., 2008). We also speculate heifers needed to learn about the positive post-ingestive influence of sequence for BFT and ALF on TF, a notion consistent with more similar scans spent foraging early in Phases 1 (BFT TF) and 2 (ALF TF), and with the consistent and marked increase in scans spent foraging on TF for animals foraging in the Phases 3 (BFT TF) and 4 (ALF TF). Our findings thus support hypotheses that complementarities and foraging sequences influence scans spent feeding and forage intake, and they are consistent with findings that intake of high-alkaloid varieties of TF and reed canarygrass both increase when sheep eat legumes high in tannins (BFT) or saponins (ALF) (Owens, 2008). While these studies provide indirect evidence of secondary compound interactions for cattle or sheep, direct evidence comes from studies where lambs given intraruminal infusions of tannins or saponins increase use of endophyte-infected TF relative to lambs not infused with tannins or saponins when offered choices of BFT, ALF, TF and OG (Lisonbee et al., 2009; Villalba et al., 2010). They also come from studies where sheep eat more when offered foods high in tannins or saponins along with foods high in alkaloids (Lyman et al., 2008). This could occur because stable complexes form between alkaloids and tannins (Okuda et al., 1982; Wong and Provenza, unpublished data), and because alkaloids bind to saponins in the gastro-intestinal tract causing their excretion in the feces (Malinow et al., 1979).
30 Scans (%) Scans (%) Scans (%) Scans (%) 17 Phase 1 Phase TF --> BFT A. B. BFT --> TF TF --> BFT BFT --> TF Phase 2 Phase C. TF --> ALF ALF --> TF D. TF --> ALF ALF --> TF Figure 2. Percent scans heifers spent grazed tall fescue (TF) before or after a meal of birdsfoot trefoil (BFT) (A and B), or alfalfa (ALF) (C and D) in 4 phases. Phases 1 and 3 lasted 10 d, whereas Phases 2 and 4 lasted 5 d. Cattle first grazed TF for 45 min followed by a meal of BFT (A and B) or ALF (C and D) for 45 min or they first grazed BFT (A and B) or ALF (C and D) for 45 min followed by TF for 45 min. Bars are standard errors.
31 18 Obviously, more experimental analyses are necessary to assess the specific physiological and behavioral effects of interactions among secondary compounds, and to better understand higher-order interactions among primary and secondary compounds in various forages (Provenza et al., 2003). Both primary and secondary compounds in too great amounts can be toxic, whereas in appropriate amounts they interact to collectively benefit both nutrition and health (Provenza and Villalba, 2006, 2010). At the most simple levels, supplemental energy and protein enhance the abilities of animals to ingest forages high in secondary compounds, particularly when animals must eat a diet high in secondary compounds (e.g., Villalba et al., 2002ab; see review by Provenza et al., 2003). In our study, additional protein in the legumes likely contributed to the differences in use of TF as additional protein helps facilitate detoxification processes (Foley et al., 1994, 1999; Illius and Jessop, 1995), and protein supplementation increases intake of fiber (Van Soest, 1994). Meal size and length is larger in dairy cows fed a supplement before eating roughage than when the roughage is fed before the supplement (Morita et al., 1996). Whatever the higher-order interactions, findings from this and past studies show that forage complementarities and sequences facilitate intake of TF undoubtedly due to complex interactions among primary and secondary compounds. IMPLICATIONS Tall fescue is the primary grass growing on more than 14 million ha of pasture- and hayland in the United States (Buckner et al., 1979). Most tall fescue is endophyte-infected, and the negative impact of tall fescue alkaloids on beef production was estimated at $600 million annually over 10 years ago (Paterson et al., 1995). A conservative estimate places the total livestock-related losses at $500 million to $1 billion a year (Univ. Nebraska, Institute of
32 19 Agriculture and Natural Resources). However, the alkaloids in TF, so problematic for ruminants, make the plant highly resistant to drought and other stresses. Improved seedling performance and survival, as well as insect and nematode resistance, drought resistance, improved nitrogen assimilation, higher seed set, and overall increased survival are all benefits from using endophyte-infected tall fescue in pasture systems (Pedersen et al., 1990). Results from our study suggest ways for developing pastures and grazing systems that incorporate a variety of plant species with different secondary compounds to increase plant survivability as well as livestock productivity when dealing with forages such as TF. If, as our results suggest, tannin- or saponin-containing legumes can partially offset the negative effects of the alkaloids in TF, then new avenues for coping with fescue toxicosis would become available to producers willing to plant mixtures of forages. Our findings thus have the potential to create positive impacts on the economic and environmental aspects of producing livestock on tall fescue pastures. REFERENCES Altman, J Observational study of behavior: Sampling methods. Behaviour 49: AOAC Official Methods of Analysis. 17th ed. Assoc. Offi. Anal. Chem., Gaithersburg, MD. Buckner, R.C., J.B. Powell, and R.V. Frakes Historical development. Pages 1-8 in Tall Fescue. R.C. Buckner, and L.P. Bush, ed. Amer. Soc. Agron., Madison, WI. Cheeke, P. R., and L. R. Shull Natural Toxicants in Feeds and Poisonous Plants. Avi Publ., Westport, CT. Foley, W. J., and C. McArthur The effects and costs of allelochemicals for mammalian
33 20 herbivores: an ecological perspective. Pages in The Digestive System in Mammals: Food, Form and Function. D.J. Chivers, and P. Langer, ed. Cambridge University Press, Cambridge, UK. Foley, W. J., G. R. Iason, and C. McArthur Role of plant secondary metabolites in the nutritional ecology of mammalian herbivores: How far have we come in 25 years? Pages in Nutritional Ecology of Herbivores. Proc. 5th Int. Symp. Nutr. Herbivores. H. G. Jung, and G. C. Fahey Jr., ed. Amer. Soc. Anim. Sci., Savoy, IL. Goering, H.K., and P.J. Van Soest Forage Fiber Analyses (Apparatus, Reagents, Procedures, and Some Applications). Agric. Handbook No ARS- USDA, Washington, DC. Hedqvist, H., I. Muller-Harvey, J.D. Reed, C.G. Krueger, and M. Murphy Characterisation of tannins and in vitro protein digestibility of several Lotus coriculatus varieties. Anim. Feed Sci. Technol. 87: Illius, A.W., and N.S. Jessop Modeling metabolic costs of allelochemical ingestion by foraging herbivores. J. Chem. Ecol. 21: Jones, W. T., and J. L. Mangan Complexes of the condensed tannins of sainfoin (Onobrychis viciifolia Scop.) with fraction 1 leaf protein and with submaxillary mucoprotein and their reversal by polyethylene glycol and ph. J. Sci. Food Agric. 28: Kumar, R., and M. Singh Tannins: their adverse role in ruminant nutrition. J. Agric. Food Chem. 32: Lee, S.T., B.L. Stegelmeier, and D.R. Gardner The isolation and identification of steroidal sapogenins in switchgrass. J. Nat. Toxins. 10:
34 21 Lisonbee, L.D., J.J. Villalba, and F.D. Provenza Effects of tannins on selection by sheep of forages containing alkaloids, tannins and saponins. J. Sci. Food Agric. 89: Lyman, T.D Livestock foraging behavior in response to interactions among alkaloids, tannins, and saponins. MS Thesis. Utah State Univ., Logan. Lyman, T.D., F.D. Provenza, and J.J. Villalba Sheep foraging behavior in response to interactions among alkaloids, tannins and saponins. J. Sci. Food Agric. 88: Malinow, M.R., P. McLaughlin, C. Stafford, A.L. Livingston, G.O. Kohler, and P.R. Cheeke Comparative effects of alfalfa saponins and alfalfa fiber on cholesterol absorption in rats. Am. J. Clin. Nutr. 32: Min, B.R., and S. P. Hart Tannins for suppression of internal parasites. J. Anim. Sci. 81: E102-E109. Morita, S., A. Ipema, and J.Metz Effect of eating sequence of concentrate and roughage on meal characteristics of roughage of cows kept in free-stall housing. Anim. Sci. Technol. 67: Mote, T. E., J. J. Villalba, and F. D. Provenza Sequence of food presentation influences intake of foods containing tannins and terpenes. Appl. Anim. Behav. Sci. 113: Okuda, T., K. Morie, and M. Shiota Effects of interaction of tannins and coexisting substances. III. Formation and solubilization of precipitates with alkaloids. J. Pharm. Soc. Japan 102: Owens, J Influence of supplemental legumes that contain tannins and saponins on intake and diet digestibility in sheep fed grasses that contain alkaloids. MS Thesis. Utah State Univ., Logan. Papachristou, T.G. L.E. Dziba, J.J. Villalba, and F.D. Provenza Patterns of diet mixing by
35 22 sheep offered foods varying in nutrients and plant secondary compounds. Appl. Anim. Behav. Sci. 108: Paterson, J., C. Forcherio, B. Larson, M. Samford, and M. Kerley The effects of fescue toxicosis on beef cattle productivity. J. Anim. Sci. 73: Pedersen, F.F., G.D. Lacefield, and D.M. Ball A review of the agronomic characteristics of endophyte-free and endophyte-infected tall fescue. Appl. Agric. Res. 5: Pedersen, M. W Relative quantity and biological activity of saponins in germinated seeds, roots, and foliage of alfalfa. Crop Sci. 15: Pedersen, M.W., D.K. Barnes, E.L. Sorensen, G.D. Griffin, M.W. Nielson, R.R. Hill, Jr., F.I. Grosheiser, R.M. Sonoda, C.H. Hanson, O.J. Hunt, R.N. Peaden, J.H. Elgin, Jr., T.E. Devine, M.J. Anderson, B.P. Goplen, L.J. Elling, and R.E. Howarth Effects of low and high saponin selection in alfalfa on agronomic and pest resistance trails and the interrelationship of these traits. Crop Sci. 16: Provenza, F. D., and J. J. Villalba Foraging in domestic vertebrates: Linking the internal and external milieu. Pages in Feeding in Domestic Vertebrates: From Structure to Function. V. L. Bels, ed. CABI Publ., Wallingford, Oxfordshire, UK. Provenza, F.D., and J.J. Villalba The role of natural plant products in modulating the immune system: An adaptable approach for combating disease in grazing animals. Small Rumin. Res. 89: Provenza, F. D., J. J. Villalba, L. E. Dziba, S. B. Atwood, and R. E. Banner Linking herbivore experience, varied diets, and plant biochemical diversity. Small Rumin. Res. 49: Rottinghaus, G.E., G.B. Garner, N.C. Creighton, and J.L. Ellis HPLC Method for quantitating
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